Evolution of Mutualism Between Globeflowers and their Pollinating Flies

Abstract

Plant/seed-eater pollinators mutualisms involve a plant pollinated by an insect whose larvae develop by eating a fraction of host-plant seeds. The outcome of the interaction therefore depends on the number of ovules fertilized by adult visits and the number of seeds destroyed by larvae. Among the very few cases of such mutualisms reported so far is the globeflower–globeflower flies mutualism, which is unique in that it involves several congeneric fly species ( Chiastocheta genus) coexisting within a single host-plant species, Trollius europaeus. These species exhibit contrasted oviposition behaviors resulting in a more or less beneficial outcome for the plant. We designed an adaptive dynamics model to investigate how morphological traits of globeflower could affect the evolution of oviposition in its pollinating flies. Three fly traits (flower age at oviposition, clutch size and the level of avoidance of already parasitized flowers) and one plant trait (closed or open corolla) were examined. Whatever the shape of the flower, evolutionary branching occurs between early and late ovipositing flies, driven by strong competition among larvae within a fruit. Once this branching occurred, the closed shape of the corolla is likely to offer a better protection to eggs of early but not of late ovipositing flies. The difference in egg survival results in higher competition among early larvae and thus selects for decreased clutch size in early flies. This can be seen as a first step in the evolution of a mutualistic behavior. The prediction of our model fits field observations of fly behavior, giving theoretical support to the hypothesis of fly sympatric speciation within its host plant. Moreover, flower closed globe shape can be positively selected in globeflowers as it results in a reduction of parasitism strength. This last evolution therefore leads to a stable mutualism between globeflowers and globeflower flies.